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Effects of the naturally occurring polyamine spermine on electrical and contractile properties of the rat portal vein were studied. 1 mM spermine nearly abolished spike activity and spontaneous contractions and decreased the intracellular Ca2+ concentration ([Ca2+]i). The phasic force responses to 0.1 and 1 microM phenylephrine were partially inhibited, but not the sustain plateau contraction caused by 5 microM phenylephrine. The Ca(2+)-force relation in high-K+ (128 mM)-depolarized veins was shifted to the right, EC50 for Ca2+ increasing from 0.50 +/- 0.03 mM (control, n = 8) to 0.65 +/- 0.06 and to 0.94 +/- 0.03 at 1 (n = 4) and 10 (n = 3) mM spermine, respectively. However, at a Ca2+ concentration of 2.5 mM, giving maximal force, there was no effect of spermine (1 mM) on either force or [Ca2+]i. Whereas extracellular spermine thus reduced contractile activity at moderate levels of stimulation, increased intracellular concentration of spermine potentiated the force response to Ca2+. Intracellular loading of spermine by reversible permeabilization increased its concentration by 2-3 times. The spontaneous activity and response to phenylephrine were unchanged. However, the Ca(2+)-force relation of depolarized veins was shifted to the left, EC50 decreasing from 0.51 +/- 0.04 mM in controls (n = 7) to 0.36 +/- 0.02 mM in the loaded veins (n = 9). Spermine increased Ca(2+)-activated force in portal veins permeabilized with beta-escin. The degree of potentiation was consistent with observed effects in spermine-loaded intact veins. The results suggest that spermine at physiological intracellular concentration may contribute to the determination of Ca2+ sensitivity in vascular smooth muscle cells.